TY - JOUR
T1 - Primary bone microanatomy records developmental aspects of life history in catarrhine primates
AU - McFarlin, Shannon C.
AU - Terranova, Carl J.
AU - Zihlman, Adrienne L.
AU - Bromage, Timothy G.
N1 - Funding Information:
This research was inspired by the groundbreaking contributions of Donald H. Enlow, particularly in his efforts to meticulously document and understand bone histodiversity and its ontogenetic foundations. One of us (S.C.M.) had the great fortune of ‘cutting teeth’ in the world of bone histology by spending innumerable hours studying the impressive comparative slide collection Enlow amassed (now curated at the New York University College of Dentistry), and this research in particular benefitted immeasurably from his feedback as a Ph.D. committee member and colleague. This work was also substantially improved through discussions with and assistance from a number of others, including Johanna Warshaw, Haviva M. Goldman, Debra Bolter, Eric Delson, Fred Szalay, and Chet Sherwood, and from students and other researchers of the Hard Tissue Research Unit, New York Consortium of Evolutionary Primatology, and the Center for the Advanced Study of Human Paleobiology at The George Washington University. We also thank Haviva Goldman, Chet Sherwood and three anonymous reviewers for helpful comments on earlier drafts of this manuscript. Skeletal materials from the Sherwood L. Washburn collection at the University of California Santa Cruz, the Museum of Comparative Zoology of Harvard University, and the Museum für Naturkunde of the Humboldt University were kindly made available for the current study; numerous individuals at these institutions also provided valuable assistance, including Maria Rutzmoser, Judy Chupasko, Manfred Ade, Peter Giere, Andrea Mess, Detlef Wilborn, and Irene Thomas. This research was supported by the National Science Foundation ( SBE-DDIG 0202823 ; funding to NYCEP), The Leakey Foundation , and the City University of New York (Robert E. Gilleece Fellowship; Dissertation Fellowship). Support to S.C.M. was also provided by funding from The George Washington University's Academic Excellence Initiative to CASHP. Partial research support was also provided by the 2010 Max Planck Research Award to T.G.B., endowed by the German Federal Ministry of Education and Research to the Max Planck Society and the Alexander von Humboldt Foundation in respect of the Hard Tissue Research Program in Human Paleobiomics.
Publisher Copyright:
© 2016 Elsevier Ltd.
PY - 2016/3/1
Y1 - 2016/3/1
N2 - A central challenge in human origins research is to understand how evolution has shaped modern human life history. As fossilized remains of our ancestors provide the only direct evidence for life history evolution, efforts to reconstruct life history in paleontological contexts have focused on hard tissues, particularly on dental development. However, among investigators of other vertebrate groups, there is a long tradition of examining primary bone microstructure to decipher growth rates and maturational timing, based on an empirical relationship between the microanatomy of primary bone and the rate at which it is deposited. We examined ontogenetic variation in primary bone microstructure at the midshaft femur of Chlorocebus aethiops, Hylobates lar, and Pan troglodytes to test whether tissue type proportions vary in accordance with predictions based on body mass growth patterns described previously. In all taxa, younger age classes were characterized by significantly higher percent areas of fibro-lamellar and/or parallel-fibered tissues, while older age classes showed significantly higher proportions of lamellar bone. In prior experimental studies, fibro-lamellar and parallel-fibered tissue types have been associated with faster depositional rates than lamellar bone. Principal components analysis revealed differences among taxa in the timing of this transition, and in the particular tissue types observed among individuals of similar dental emergence status. Among M1 and M2 age classes, higher proportions of parallel-fibered and fibro-lamellar tissues were observed in those taxa characterized by reportedly faster body mass growth rates. Further, persistence of fibro-lamellar tissue throughout DECID, M1 and M2 age classes in chimpanzees contrasts with the pattern reported previously for modern humans. Despite the necessary limitations of our cross-sectional study design and the secondary remodeling of bone in primates, large areas of primary bone remain intact and represent a valuable and independent source of information about the evolution of growth and development in the fossil record.
AB - A central challenge in human origins research is to understand how evolution has shaped modern human life history. As fossilized remains of our ancestors provide the only direct evidence for life history evolution, efforts to reconstruct life history in paleontological contexts have focused on hard tissues, particularly on dental development. However, among investigators of other vertebrate groups, there is a long tradition of examining primary bone microstructure to decipher growth rates and maturational timing, based on an empirical relationship between the microanatomy of primary bone and the rate at which it is deposited. We examined ontogenetic variation in primary bone microstructure at the midshaft femur of Chlorocebus aethiops, Hylobates lar, and Pan troglodytes to test whether tissue type proportions vary in accordance with predictions based on body mass growth patterns described previously. In all taxa, younger age classes were characterized by significantly higher percent areas of fibro-lamellar and/or parallel-fibered tissues, while older age classes showed significantly higher proportions of lamellar bone. In prior experimental studies, fibro-lamellar and parallel-fibered tissue types have been associated with faster depositional rates than lamellar bone. Principal components analysis revealed differences among taxa in the timing of this transition, and in the particular tissue types observed among individuals of similar dental emergence status. Among M1 and M2 age classes, higher proportions of parallel-fibered and fibro-lamellar tissues were observed in those taxa characterized by reportedly faster body mass growth rates. Further, persistence of fibro-lamellar tissue throughout DECID, M1 and M2 age classes in chimpanzees contrasts with the pattern reported previously for modern humans. Despite the necessary limitations of our cross-sectional study design and the secondary remodeling of bone in primates, large areas of primary bone remain intact and represent a valuable and independent source of information about the evolution of growth and development in the fossil record.
KW - Apes
KW - Bone histology
KW - Growth and development
KW - Life history
KW - Old World monkeys
UR - http://www.scopus.com/inward/record.url?scp=84960158410&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84960158410&partnerID=8YFLogxK
U2 - 10.1016/j.jhevol.2015.12.004
DO - 10.1016/j.jhevol.2015.12.004
M3 - Article
C2 - 26989017
AN - SCOPUS:84960158410
SN - 0047-2484
VL - 92
SP - 60
EP - 79
JO - Journal of Human Evolution
JF - Journal of Human Evolution
ER -